Highlights • Phenotyping technology can increase the throughput of plant screening in the field. • Early season detection of plant diseases is key to reducing crop yield losses. • Disease diagnosis relies on symptom recognition through observations and ratings. • Remote sensing methods can identify, quantify and monitor plant diseases. • Sensor-based phenotyping will accelerate the rate of genetic gain in crops. Effective implementation of technology that facilitates accurate and high-throughput screening of thousands of field-grown lines is critical for accelerating crop improvement and breeding strategies for higher yield and disease tolerance. Progress in the development of field-based high throughput phenotyping methods has advanced considerably in the last 10 years through technological progress in sensor development and high-performance computing. Here, we review recent advances in high throughput field phenotyping technologies designed to inform the genetics of quantitative traits, including crop yield and disease tolerance. Successful application of phenotyping platforms to advance crop breeding and identify and monitor disease requires: (1) high resolution of imaging and environmental sensors; (2) quality data products that facilitate computer vision, machine learning and GIS; (3) capacity infrastructure for data management and analysis; and (4) automated environmental data collection. Accelerated breeding for agriculturally relevant crop traits is key to the development of improved varieties and is critically dependent on high-resolution, high-throughput field-scale phenotyping technologies that can efficiently discriminate better performing lines within a larger population and across multiple environments.

Summary Maize grows on every continent save Antarctica and provides food and biofuels for millions of people. Now, researchers studying ancient and modern maize have found a clue to its popularity over the millennia: maize’s easily adjustable flowering time, which enabled ancient peoples to get the plant to thrive in diverse climates, according to several studies presented in July at the meeting of the Society for Molecular Biology and Evolution in Austin. The studies found hints of the genomic shifts behind such rapid change, and ancient DNA studies presented at the meeting began to clarify when maize flowering came under farmer control, revealing enormous adaptive potential that humans were able to exploit.

To defend against extracellular pathogens, plants primarily depend on cell-autonomous innate immunity due to the lack of the circulatory immune system including mobile immune cells. To extracellularly restrict or kill the pathogens, plant cells dump out antimicrobials. However, since antimicrobials are also toxic to plant cells themselves, they have to be safely delivered to the target sites in a separate vesicular compartment. In addition, because immune responses often requires energy otherwise used for the other metabolic processes, it is very important to properly control the duration and strength of immune responses depending on pathogen types. This can be achieved by regulating the sensing of immune signals and the delivery/discharge of extracellular immune molecules, all of which are controlled by membrane trafficking in plant cells. Soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) are now considered as the minimal factors that can merge two distinct membranes of cellular compartments. Hence, in this review, known and potential immune functions of SNAREs as well as regulatory proteins will be discussed.

Both plants and animals rely on nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins to respond to invading pathogens and activate immune responses. An emerging concept of NLR function is that “sensor” NLR proteins are paired with “helper” NLRs to mediate immune signaling. However, our fundamental knowledge of sensor/helper NLRs in plants remains limited. In this study, we discovered a complex NLR immune network in which helper NLRs in the NRC (NLR required for cell death) family are functionally redundant but display distinct specificities toward different sensor NLRs that confer immunity to oomycetes, bacteria, viruses, nematodes, and insects. The helper NLR NRC4 is required for the function of several sensor NLRs, including Rpi-blb2, Mi-1.2, and R1, whereas NRC2 and NRC3 are required for the function of the sensor NLR Prf. Interestingly, NRC2, NRC3, and NRC4 redundantly contribute to the immunity mediated by other sensor NLRs, including Rx, Bs2, R8, and Sw5. NRC family and NRC-dependent NLRs are phylogenetically related and cluster into a well-supported superclade. Using extensive phylogenetic analysis, we discovered that the NRC superclade probably emerged over 100 Mya from an NLR pair that diversified to constitute up to one-half of the NLRs of asterids. These findings reveal a complex genetic network of NLRs and point to a link between evolutionary history and the mechanism of immune signaling. We propose that this NLR network increases the robustness of immune signaling to counteract rapidly evolving plant pathogens.

Climate change has been reported as a driver for emerging food and feed safety issues worldwide and its expected impact on the presence of mycotoxins in food and feed is of great concern. Aflatoxins have the highest acute and chronic toxicity of all mycotoxins; hence, the maximal concentration in agricultural food and feed products and their commodities is regulated worldwide. The possible change in patterns of aflatoxin occurrence in crops due to climate change is a matter of concern that may require anticipatory actions. The aim of this study was to predict aflatoxin contamination in maize and wheat crops, within the next 100 years, under a +2 °C and +5 °C climate change scenario, applying a modelling approach. Europe was virtually covered by a net, 50 × 50 km grids, identifying 2254 meshes with a central point each. Climate data were generated for each point, linked to predictive models and predictions were run consequently. Aflatoxin B1 is predicted to become a food safety issue in maize in Europe, especially in the +2 °C scenario, the most probable scenario of climate change expected for the next years. These results represent a supporting tool to reinforce aflatoxin management and to prevent human and animal exposure.

A transient rise in cytosolic calcium ion concentration is one of the main signals used by plants in perception of their environment. The role of calcium in the detection of abiotic stress is well documented; however, its role during biotic interactions remains unclear. Here, we use a fluorescent calcium biosensor (GCaMP3) in combination with the green peach aphid (Myzus persicae) as a tool to study Arabidopsis thaliana calcium dynamics in vivo and in real time during a live biotic interaction. We demonstrate rapid and highly localized plant calcium elevations around the feeding sites of M. persicae, and by monitoring aphid feeding behavior electrophysiologically, we demonstrate that these elevations correlate with aphid probing of epidermal and mesophyll cells. Furthermore, we dissect the molecular mechanisms involved, showing that interplay between the plant defense coreceptor BRASSINOSTEROID INSENSITIVE-ASSOCIATED KINASE1 (BAK1), the plasma membrane ion channels GLUTAMATE RECEPTOR-LIKE 3.3 and 3.6 (GLR3.3 and GLR3.6), and the vacuolar ion channel TWO-PORE CHANNEL1 (TPC1) mediate these calcium elevations. Consequently, we identify a link between plant perception of biotic threats by BAK1, cellular calcium entry mediated by GLRs, and intracellular calcium release by TPC1 during a biologically relevant interaction.

Arbuscular mycorrhizas (AM) are the most common symbiotic associations between plant's root compartment and fungi. They provide nutritional benefit (mostly inorganic phosphate, Pi) leading to improved growth, and non-nutritional benefits including defense responses to environmental cues throughout the host plant, which in return delivers carbohydrates to the symbiont. However, how transcriptional and metabolic changes occurring in leaves of AM plants differ from those induced by Pi fertilization is poorly understood. We investigated systemic changes in the leaves of mycorrhized Medicago truncatula in conditions with no improved Pi status, and compared them with those induced by high Pi treatment in non-mycorrhized plants. Microarray-based genome-wide profiling indicated upregulation by mycorrhization of genes involved in flavonoid, terpenoid, jasmonic acid (JA) and abscisic acid (ABA) biosynthesis as well as enhanced expression of MYC2, the master regulator of JA-dependent responses. Accordingly, total anthocyanins and flavonoids increased, and most flavonoid species were enriched in AM-leaves. Both the AM- and Pi treatment co-repressed iron homeostasis genes resulting in lower levels of available iron in leaves. In addition, higher levels of cytokinins were found in leaves of AM- and Pi-treated plants whereas the level of ABA was specifically increased in AM-leaves. Treatment of non-mycorrhized plants with either ABA or JA induced upregulation of MYC2, whereas JA also induced upregulation of flavonoid and terpenoid biosynthetic genes. Based on these results, we propose that mycorrhization and Pi fertilization share cytokinin-mediated improved shoot growth, whereas enhanced ABA biosynthesis and JA-regulated flavonoid and terpenoid biosynthesis in leaves is specific to mycorrhization.

One of the most common challenges for both conventional and modern crop improvement is that the appearance of one desirable trait in a new crop variety is always balanced by the impairment of one or more other beneficial characteristics. The best way to overcome this problem is the flexible utilization of regulatory genes, especially genes that provide more efficient and precise regulation in a targeted manner. MicroRNAs (miRNAs), a type of short non-coding RNA, are promising candidates in this area due to their role as master modulators of gene expression at the post-transcriptional level, targeting messenger RNAs for cleavage or directing translational inhibition in eukaryotes. We herein highlight the current understanding of the biological role of miRNAs in orchestrating distinct agriculturally important traits by summarizing recent functional analyses of 65 miRNAs in 9 major crops worldwide. The integration of current miRNA knowledge with conventional and modern crop improvement strategies is also discussed.

Modern wheat, which underlies the diet of many across the globe, has a long history of selection and crosses among different species. Avni et al. used the Hi-C method of genome confirmation capture to assemble and annotate the wild allotetraploid wheat ( Triticum turgidum ). They then identified the putative causal mutations in genes controlling shattering (a key domestication trait among cereal crops). They also performed an exome capture–based analysis of domestication among wild and domesticated genotypes of emmer wheat. The findings present a compelling overview of the emmer wheat genome and its usefulness in an agricultural context for understanding traits in modern bread wheat.

In plants the hormone jasmonic acid (JA) is synthesized in response to attack by pathogens and herbivores, leading to activation of defense responses. Rapidly following JA accumulation the hormone is metabolized, presumably to prevent inhibitive effects of high JA levels on growth and development. The enzymes that directly inactivate JA were so far unknown. Here, we identify four jasmonate-induced oxygenases (JOXs) in Arabidopsis that hydroxylate jasmonic acid to form inactive 12-OH-JA. A mutant that no longer produces the four enzymes hyperaccumulates JA, exhibits reduced growth, and is highly resistant to attackers that are sensitive to JA-dependent defense. The JOX enzymes thus play an important role in determining the amplitude and duration of JA responses to balance the growth–defense trade-off.

Nitrate plays an essential role during plant development as nutrient and also as signal molecule, in both cases working via the activity of nitrate transporters. To date, few studies on NRT2 or NPF nitrate transporters in legumes have been reported, and most of those concern Lotus japonicus and Medicago truncatula. A molecular characterization led to the identification of 4 putative LjNRT2 and 37 putative LjNPF gene sequences in L. japonicus. In M. truncatula, the NRT2 family is composed of 3 putative members. Using the new genome annotation of M. truncatula (Mt4.0), we identified, for this review, 97 putative MtNPF sequences, including 32 new sequences relative to previous studies. Functional characterization has been published for only two MtNPF genes, encoding nitrate transporters of M. truncatula. Both transporters have a role in root system development via abscisic acid signaling: MtNPF6.8 acts as a nitrate sensor during the cell elongation of the primary root, while MtNPF1.7 contributes to the cellular organization of the root tip and nodule formation. An in silico expression study of MtNPF genes confirmed that NPF genes are expressed in nodules, as previously shown for L. japonicus, suggesting a role for the corresponding proteins in nitrate transport, or signal perception in nodules. This review summarizes our knowledge of legume nitrate transporters and discusses new roles for these proteins based on recent discoveries.

The plant hormone cytokinin affects a diverse array of growth and development processes and responses to the environment. How a signaling molecule mediates such a diverse array of outputs and how these response pathways are integrated with other inputs remain fundamental questions in plant biology. To this end, we characterized the transcriptional network initiated by the type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs) that mediate the cytokinin primary response, making use of chromatin immunoprecipitation sequencing (ChIP-seq), protein-binding microarrays, and transcriptomic approaches. By ectopic overexpression of ARR10, Arabidopsis lines hypersensitive to cytokinin were generated and used to clarify the role of cytokinin in regulation of various physiological responses. ChIP-seq was used to identify the cytokinin-dependent targets for ARR10, thereby defining a crucial link between the cytokinin primary-response pathway and the transcriptional changes that mediate physiological responses to this phytohormone. Binding of ARR10 was induced by cytokinin with binding sites enriched toward the transcriptional start sites for both induced and repressed genes. Three type-B ARR DNA-binding motifs, determined by use of protein-binding microarrays, were enriched at ARR10 binding sites, confirming their physiological relevance. WUSCHEL was identified as a direct target of ARR10, with its cytokinin-enhanced expression resulting in enhanced shooting in tissue culture. Results from our analyses shed light on the physiological role of the type-B ARRs in regulating the cytokinin response, mechanism of type-B ARR activation, and basis by which cytokinin regulates diverse aspects of growth and development as well as responses to biotic and abiotic factors.

Alleles that confer multiple disease resistance (MDR) are valuable in crop improvement, although the molecular mechanisms underlying their functions remain largely unknown. A quantitative trait locus, qMdr9.02, associated with resistance to three important foliar maize diseases—southern leaf blight, gray leaf spot and northern leaf blight—has been identified on maize chromosome 9. Through fine-mapping, association analysis, expression analysis, insertional mutagenesis and transgenic validation, we demonstrate that ZmCCoAOMT2, which encodes a caffeoyl-CoA O-methyltransferase associated with the phenylpropanoid pathway and lignin production, is the gene within qMdr9.02 conferring quantitative resistance to both southern leaf blight and gray leaf spot. We suggest that resistance might be caused by allelic variation at the level of both gene expression and amino acid sequence, thus resulting in differences in levels of lignin and other metabolites of the phenylpropanoid pathway and regulation of programmed cell death.

Floral organ identities in plants are specified by the combinatorial action of homeotic master regulatory transcription factors. How these factors achieve their regulatory specificities is however still largely unclear. Genome-wide in vivo DNA binding data show that homeotic MADS-domain proteins recognize partly distinct genomic regions, suggesting that DNA binding specificity contributes to functional differences of homeotic protein complexes. We used in vitro systematic evolution of ligands by exponential enrichment followed by high throughput DNA sequencing (SELEX-seq) on several floral MADS-domain protein homo- and heterodimers to measure their DNA-binding specificities. We show that specification of reproductive organs is associated with distinct binding preferences of a complex formed by SEPALLATA3 (SEP3) and AGAMOUS (AG). Binding specificity is further modulated by different binding site spacing preferences. Combination of SELEX-seq and genome-wide DNA binding data allows to differentiate between targets in specification of reproductive versus perianth organs in the flower. We validate the importance of DNA-binding specificity for organ-specific gene regulation by modulating promoter activity through targeted mutagenesis. Our study shows that intrafamily protein interactions affect DNA-binding specificity of floral MADS-domain proteins. Differential DNA-binding of MADS-domain protein complexes plays a role in the specificity of target gene regulatio

The members of the pathogenesis-related protein 1 (PR-1) family are among the most abundantly produced proteins in plants on pathogen attack, and PR-1 gene expression has long been used as a marker for salicylic acid-mediated disease resistance. However, despite considerable interest over several decades, their requirement and role in plant defence remains poorly understood. Recent reports have emerged demonstrating that PR-1 proteins possess sterol-binding activity, harbour an embedded defence signalling peptide, and are targeted by plant pathogens during host infection. These studies have re-energised the field and provided long-awaited insights into a possible PR-1 function. Here we review the current status of PR-1 proteins and discuss how these recent advances shed light on putative roles for these enigmatic proteins. Trends

Recent studies have shown that plant pathogenesis-related protein 1 (PR-1) family members bind sterols. This function is responsible for antimicrobial activity towards sterol auxotrophs such as Phytophthora species. However, the link between sterol binding and the proposed broader antimicrobial function of PR-1 remains unclear.

PR-1 proteins harbour an embedded C-terminal peptide (CAPE) involved in plant immune signalling. Evidence suggests that CAPE has a signalling role that facilitates defence responses against microbial pathogens and also herbivores. The CAPE response is independent of other defence signalling pathways such as those elicited by recognised pathogen-associated molecular patterns.

The significance of PR-1 proteins during plant–microbe interactions is now realised, with a growing list of identified pathogen effector proteins that directly interact with PR-1 during infection.

Retrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding. To ensure genome integrity several silencing mechanisms have evolved to repress retrotransposon mobility. Even though retrotransposons fully depend on transcriptional activity of the host RNA polymerase II (Pol II) for their mobility, it was so far unclear whether Pol II is directly involved in repressing their activity. Here we show that plants defective in Pol II activity lose DNA methylation at repeat sequences and produce more extrachromosomal retrotransposon DNA upon stress in Arabidopsis and rice. We demonstrate that combined inhibition of both DNA methylation and Pol II activity leads to a strong stress-dependent mobilization of the heat responsive ONSEN retrotransposon in Arabidopsis seedlings. The progenies of these treated plants contain up to 75 new ONSEN insertions in their genome which are stably inherited over three generations of selfing. Repeated application of heat stress in progeny plants containing increased numbers of ONSEN copies does not result in increased activation of this transposon compared to control lines. Progenies with additional ONSEN copies show a broad panel of environment-dependent phenotypic diversity. We demonstrate that Pol II acts at the root of transposon silencing. This is important because it suggests that Pol II can regulate the speed of plant evolution by fine-tuning the amplitude of transposon mobility. Our findings show that it is now possible to study induced transposon bursts in plants and unlock their use to induce epigenetic and genetic diversity for crop breeding.

Wheat blast first emerged in Brazil in the mid-1980s and has recently caused heavy crop losses in Asia. Here we show how this devastating pathogen evolved in Brazil. Genetic analysis of host species determinants in the blast fungus resulted in the cloning of avirulence genes PWT3 and PWT4, whose gene products elicit defense in wheat cultivars containing the corresponding resistance genes Rwt3 and Rwt4. Studies on avirulence and resistance gene distributions, together with historical data on wheat cultivation in Brazil, suggest that wheat blast emerged due to widespread deployment of rwt3 wheat (susceptible to Lolium isolates), followed by the loss of function of PWT3. This implies that the rwt3 wheat served as a springboard for the host jump to common wheat.

Plants respond to microbial attack with a lethal burst of reactive oxygen species. How then, do pathogens successfully invade plants? Unexpectedly, a link between primary metabolism and suppression of plant immunity allows the rice blast fungus Magnaporthe oryzae to grow in such a hostile environment.

Plant-infecting fungi and oomycetes are an ever present threat to global food security — each year they destroy sufficient food to feed half a billion people1. Understanding how these pathogens infect and colonize host plants is therefore crucial if we are to develop new strategies to fight fungal diseases and improve plant health. The rice blast fungus Magnaporthe oryzae is responsible for the most devastating disease of cultivated rice, the primary staple for more than half of the world's population2. Strains of the same fungus also cause blast disease of wheat, a new disease that is currently causing a severe outbreak in Bangladesh and India3. Because of its economic significance and genetic tractability, rice blast disease has also emerged as a major model for studying the molecular and cellular basis of fungal infection2,4. Similar to many pathogenic fungi, M. oryzae has evolved highly sophisticated ways to invade plant cells and disable their defence systems.

One of the earliest responses of plants to microbial attack is the induction of a rapid, transient burst of reactive oxygen species5 (ROS). This oxidative burst is a potent defence reaction that will kill any unsuspecting microorganism. How can pathogens still successfully invade plant cells and contend with such high concentrations of ROS? In this issue of Nature Microbiology, Marroquin-Guzman and colleagues report that a link between primary fungal metabolism and the suppression of plant immunity enables M. oryzae to protect itself from nitrooxidative stress and maintain redox balance within living rice cells6, thereby facilitating its growth within such a hostile environment.

To initiate rice infection, a fungal spore adheres tightly to the rice leaf surface, germinates, and rapidly elaborates a specialized infection structure called an appressorium that is used to breach the tough outer leaf cuticle4. Once inside a host cell, the fungus develops bulbous, branched hyphae that maintain intimate contact with the plasma membrane of the living plant cell, forming a specialized biotrophic interfacial complex7. The pathogen and host then engage in an intense molecular dialogue; plant metabolism is reprogrammed to the pathogen's benefit and the host immune response is suppressed4,7. Much recent research has focused on fungal effector proteins, a highly diverse group of secreted molecules that target immune responses in the host to facilitate pathogen infection and spread8. However, fungi have clearly evolved additional ways to keep plant defences at bay. Marroquin-Guzman and colleagues identified and characterized nitronate monooxygenase (NMO) from M. oryzae, an enzyme normally used by fungal cells to protect themselves from nitrooxidative stress6. They show, however, that NMO is also required for utilization of nitrate and nitrite as nitrogen sources and for maintaining redox balance within living rice cells during pathogen colonization. The latter role of NMO is essential for pathogenicity, because it provides a novel mechanism by which the fungus can prevent elicitation of the plant oxidative burst (Fig. 1).

Vitamin A deficiency remains one of the world's major public health problems despite food fortification and supplements strategies. Biofortification of staple crops with enhanced levels of pro-vitamin A (PVA) offers a sustainable alternative strategy to both food fortification and supplementation. As a proof of concept, PVA-biofortified transgenic Cavendish bananas were generated and field trialed in Australia with the aim of achieving a target level of 20 μg/g of dry weight (dw) β-carotene equivalent (β-CE) in the fruit. Expression of a Fe'i banana-derived phytoene synthase 2a (MtPsy2a) gene resulted in the generation of lines with PVA levels exceeding the target level with one line reaching 55 μg/g dw β-CE. Expression of the maize phytoene synthase 1 (ZmPsy1) gene, used to develop ‘Golden Rice 2’, also resulted in increased fruit PVA levels although many lines displayed undesirable phenotypes. Constitutive expression of either transgene with the maize polyubiquitin promoter increased PVA accumulation from the earliest stage of fruit development. In contrast, PVA accumulation was restricted to the late stages of fruit development when either the banana 1-aminocyclopropane-1-carboxylate oxidase or the expansin 1 promoters were used to drive the same transgenes. Wild-type plants with the longest fruit development time had also the highest fruit PVA concentrations. The results from this study suggest that early activation of the rate-limiting enzyme in the carotenoid biosynthetic pathway and extended fruit maturation time are essential factors to achieve optimal PVA concentrations in banana fruit.

Volatile organic compounds (VOCs) serve as invisible lines of communication among host plants, pathogens, commensals, community groups, and, with flowers, their pollinators. Studying petunia flowers, Adebesin et al. show that VOCs do not passively diffuse out of the cells but are actively shuttled across the plasma membrane by an ABC (ATP-binding cassette) transporter (see the Perspective by Eberl and Gershenzon). Disabling the transporter results in damage to the cell's membranes by intracellular accumulation of VOCs.

Plants live in association with microorganisms, which are well known as a rich source of specialized metabolites, including volatile compounds. The increasing numbers of described plant microbiomes allowed manifold phylogenetic tree deductions, but less emphasis is presently put on the metabolic capacities of plant-associated microorganisms. With the focus on small volatile metabolites we summarize i) the knowledge of prominent bacteria of plant microbiomes, ii) present the state-of-the-art of individual (discrete) microbial organic and inorganic volatiles affecting plants and fungi, and iii) emphasize the high potential of microbial volatiles in mediating microbe-plant interactions. So far, 94 discrete organic and five inorganic compounds were investigated, most of them trigger alterations of the growth, physiology and defense responses in plants and fungi but little is known about the specific molecular and cellular targets. Large overlaps in emission profiles of the emitters and receivers render specific VOC-mediated interactions highly unlikely for most bioactive mVOCs identified so far.

Wheat (Triticum aestivum L.) incurs significant yield losses from powdery mildew, a major fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). enhanced disease resistance1 (EDR1) plays a negative role in the defense response against powdery mildew in Arabidopsis thaliana; however, the edr1 mutant does not show constitutively activated defense responses. This makes EDR1 an ideal target for approaches using new genome-editing tools to improve resistance to powdery mildew. We cloned TaEDR1 from hexaploid wheat and found high similarity among the three homoeologs of EDR1. Knock-down of TaEDR1 by virus-induced gene silencing or RNA interference enhanced resistance to powdery mildew, indicating that TaEDR1 negatively regulates powdery mildew resistance in wheat. We used CRISPR/Cas9 technology to generate Taedr1 wheat plants by simultaneous modification of the three homoeologs of wheat EDR1. No off-target mutations were detected in the Taedr1 mutant plants. The Taedr1 plants were resistant to powdery mildew and did not show mildew-induced cell death. Our study represents the successful generation of a potentially valuable trait using genome-editing technology in wheat and provides germplasm for disease resistance breeding.

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